Rodriguésia 62(4): 927-936. 2011 http://rodriguesia.jbrj.gov.br

Morpho-anatomical adaptations of polygonus () to lotic and lentic environments Adaptações morfo-anatômicas de Potamogeton polygonus aos ambientes lêntico e lótico

Makeli Garibotti Lusa1, Maria Regina Torres Boeger1, Maria Cecília de Chiara Moço2 & Cleusa Bona1

Abstract Aquatic macrophytes show great phenotypic plasticity and are able to occupy environments with different physicochemical conditions. The present study aimed to characterize morphology and anatomical structure of the pondweed, Potamogeton polygonus Cham. & Schltdl., and to identify adaptive modifications of the in lotic and lentic environments. Sampling was carried out in Palmas and General Carneiro, Paraná state, southern Brazil. Ten individuals from each locality were collected. Morpho-anatomical characteristics of the roots, stems and leaves were measured. The anatomical structure was analyzed with light microscopy and scanning electron microscopy. Significant morphological and anatomical adaptive differences were observed between of the two environments. Key words: anatomy, , morphology, phenotypic plasticity, Potamogeton. Resumo Plantas aquáticas apresentam grande plasticidade fenotípica, sendo capazes de ocupar ambientes com diferentes condições físico-químicas da água. O objetivo deste trabalho é caracterizar a morfologia e a estrutura anatômica de Potamogeton polygonus Cham. & Schltdl., e identificar as alterações adaptativas da espécie em ambientes lêntico e lótico. As coletas foram realizadas nos municípios de Palmas e General Carneiro, Estado do Paraná, Brasil. Foram coletados dez indivíduos em cada localidade e realizadas mensurações de parâmetros morfológicos e anatômicos de raizes, caules e folhas. A estrutura anatômica foi analisada em microscopia fotônica e eletrônica de varredura. Foram constatadas modificações morfológicas e anatômicas de potencial papel adaptativo entre as plantas dos dois ambientes. Palavras-chave: anatomia, morfologia, planta aquática, plasticidade fenotípica, Potamogeton.

Introduction Rodrigues & Irgang (2001) point out the large Aquatic plants are constantly subjected to a morphological variation among Brazilian species of wide variety of environmental factors, which vary Potamogeton L. Kaplan (2002) recorded the at continental scale (e.g. according to latitude and morphological plasticity of 41 experimentally longitude) (Santamaría et al. 2003), as well as at cultivated species of Potamogeton from several parts local scale (e.g. light, temperature, salinity, flow of the world. The target species of most studies is P. velocity etc.) (Santamaría 2002). Many widely pectinatus L. Due to its wide geographic distribution, distributed aquatic species are able to respond plastic responses of this species have already been plastically to diverse conditions (Santamaría 2002). reported in relation to temperature (Spencer 1986), Studies showed that even clonal populations of solar radiation ( Pilon & Santamaría 2002b), nutrient aquatic plants, which have low genetic variability, availability in the sediment, wave turbulence can exhibit compensatory plastic responses on (Idestam-Almquist & Kautsky 1995) and latitude environmental gradients (Grace 1993). The ability (Pilon & Santamaría 2002a; Santamaría et al. 2003). of an organism to change its morphology and The species P. polygonus Cham. & Schltdl. physiology in response to environmental is widely distributed in South America, in lentic conditions is known as phenotypic plasticity and lotic fresh waters (Rodrigues & Irgang 2001). (Via et al. 1995). Rodrigues & Irgang (2001) reported that this species

1 Universidade Federal do Paraná, Depto. Botânica, Setor Ciências Biológicas, Campus 3 (Centro Politécnico), 81531-990, CP 19031, Curitiba, PR, Brazil. [email protected]. 2 Universidade Federal do Rio Grande do Sul, Instituto de Biociências, Depto. Botânica, 91509-900, Porto Alegre, RS, Brazil. 928 Lusa, M.G. et al. exhibits large variation in leaf width, which may digitalized images in the program Sigma Scan Pro lead to error in taxonomic identification. However, (version 5.0, SPSS Inc., Chicago IL, USA). there is no analysis of morphological and anatomical For the quantitative anatomy analysis, we variations in this species. Wiegleb (1990) used samples from the same plants used for the highlighted the importance of anatomical characters morphological analysis. From each individual we for the systematics of the genus, but only Alix & collected samples of root (apex to the tenth node), Scribailo (2006) and Kaplan (2001) used this stem and leaves (at the middle third of the leaf approach to distinguish species and hybrids. from the fifth node). Samples were fixed in FAA The present study aimed to characterize the 50 (Johansen 1940), and preserved in 70% morphology and anatomical structure of the ethanol. Semi-permanent slides were assembled vegetative organs of P. polygonus and to identify from freehand slices with razor blade, stained with the adaptive variations of this plant in lentic and toluidine blue and mounted in glycerinated lotic environments. gelatin (Roeser 1972; Berlyn & Miksche 1976). Permanent slides were made from samples Material and Methods included in hydroxyethylmethacrylate resin, Two study populations were chosen, which sectioned in a rotation microtome, stained with were subjected to different conditions of water toluidine blue (O’Brien et al. 1965), and mounted velocity: 1) lotic environment - Arroio do Neno in synthetic resin (Permount). The lacunal areas (26° 21’06.2’’S ; 51°36’51.6’’W), located at Lajeado of the stem and leaf mesophyll were measured Grande Farm, Palmas, state of Paraná, Iguaçú River from digital images of the abenchyma. Others Basin, a river composed mostly of water flowing anatomical parameters were measured: number over rocks, with deeper backwater areas; and 2) of fiber bundles in the stem and in the leaf blade, lentic environment – in dam 15, São Pedro Farm, General and in the thickness of their cell wall fibers; the Carneiro, state of Paraná (26° 22’28.8’’S; 51°21’29.3’’W), thickness of the leaf in the central region and an area with argillaceous sediment, shallower near mesophyll; the thickness of the cell wall of the root the edges and deeper in the middle. exodermis and the leaf epiderms. Microscopic In each environment, water depth was analyses and photomicrographic records were made measured at the deepest point and physico- under photonic and stereoscopic microscopes chemical parameters of the water were assessed (ZEISS Axiolab), with a digital camera attached. at 10 cm below the surface. Temperature, oxygen For the analysis of leaf and stem surfaces level (in % and mg/l) and pH were measured with and of the aerenchyma, samples of leaf and stem a multi-parameter analyzer Consort C535. Water were observed under scanning electron velocity was measured with Flow Probe FP101. microscopy. The samples were dehydrated in

Voucher material was deposited in the herbarium absolute ethanol and critical point dried with CO2, UPCB, Botany Department, Universidade Federal in the equipment BAL-TEC CPD 030, were adhered do Paraná, Curitiba, state of Paraná, southern Brazil, to metallic supports with adhesive copper tape, and assigned numbers UPCB 65092 (lotic coated with gold in the equipment Balzers SCD 030, environment) and UPCB 61311 (lentic environment). and analyzed under scanning electron microscopy For the quantitative morphology analysis, ten Jeol 6360LV, at the Center for Scanning Electron fully developed individuals were collected in each Microscopy of Universidade Federal do Paraná. population. We measured total plant height and In order to test for differences between internode length of all individuals. Stem diameter specimens growing in lentic and lotic environments, was always measured along its longest axis, due to data were submitted to an analysis of variance flattened shape. From the fifth apical node on, we (ANOVA) and averages were submitted to a Student’s removed five (5) leaves from each plant, which were t-test (significance level of 5%) in MStat 5.2. then pressed and oven-dried at 60 ºC. For these leaves, we measured maximum values of leaf blade Results length and leaf blade width, as well as leaf area; we also calculated the arithmetic mean per individual Study area for each variable. Measurements of leaf blade length Water abiotic parameters measured in each and width were taken with a digital caliper (0.01 mm environment are presented in Table 1. The lentic resolution). Leaf area was calculated using environment is five times deeper than the lotic, which

Rodriguésia 62(4): 927-936. 2011 Morpho-anatomical adaptations of Potamogeton polygonus 929 probably affects its velocity, which is 27 times lower. elements are in direct contact with the endodermis Electrical conductivity and dissolved salts were (Fig. 1c). No structural difference in the vascular higher in the lentic environment, whereas dissolved cylinder was observed between plants of the two oxygen was higher in the lotic environment. In both environments. sites pH was similar, varying from 7.2 to 7.4. Stem – The transverse section of this organ Morphology is elliptical. The epidermis exhibits square-shaped Potamogeton polygonus plants are perennial cells (Fig. 1d) with chloroplasts and a thickened and fixed-submersed herbs, with short internodes outer periclinal wall, with occasional epicuticular and linear, membranous, and parallel-nerved leaves striations. The cortex is composed of a subepidermal with acuminate apex, truncate and sessile base, with layer of parenchyma cells with chloroplasts, stipule convolute and senescent. Plant morphology interspersed by fiber bundles and aerenchyma, with varied significantly between individuals of the lentic the cells arranged in a honeycomb (Fig. 1d). The and lotic environments (Table 2). The plants from the aerenchyma lacunae are divided transversally by lotic environment had lower values of leaf blade, leaf uniseriate diaphragms formed by arm-shaped cells area, length between internodes and total plant height, (Fig. 1e-g). The cells that limit the air lacunae and but they had larger stem diameters. Plants from lotic those that compose the diaphragm have and lentic environments did not differ significantly chloroplasts. No difference in aerenchyma pattern from each other in terms of leaf blade width. or percentage of lacunal area was recorded between plants from the two environments (Table 3). Fiber Anatomy bundles also appear scattered among the Root – In the absorption zone, common parenchyma cells of the aerenchyma. There was no epidermal cells have an outer periclinal wall that is difference in the total number of fiber bundles, but convex and root hairs are positioned in front of the the walls of these fibers were thicker in the lotic exodermal passage cells (Fig. 1a-b). At the end of environment (Table 3). The walls of endodermal the absorption zone, epidermal cells are eliminated cells, in the younger portions of the stem, have leaving the exodermis exposed. The biseriate only Casparian strips, but in the completely hypodermis is composed of one layer of exodermis developed internodes they undergo thickening and and other layer of parenchyma cells (Fig. 1a). The lignification. The vascular cylinder is oblong in exodermis has cells with thick walls and passage transverse section, with four to six vascular bundles: cells with thin walls (Fig. 1b). Wall thickness of the two larger in the center and two smaller on each exodermal cells was greater in the lotic environment side, without pith formation (Fig. 1h). Both central (Table 3). The aerenchyma resembles a radial and lateral bundles can exhibit fusion. Vascular lysigenous type; the lacunae are limited by radial bundles exhibit large lacunae of protoxylem, large septa (Fig. 1a). The inner region of the cortex is phloem sieve elements and are partially surrounded formed by approximately five layers of parenchyma by fibers. The vascular cylinder structure is similar cells with intercellular spaces, and internally by the in both environments. endodermis (Fig. 1c). The endodermal cells, in the proximal region of the root, has secondary wall Leaf – The epidermis is uniseriate and thickening in O-shape and distinguishable passage chlorophyllous, and in the lotic environment the cells. The vascular cylinder is pentarch, the outer periclinal walls are thicker (Table 3; Fig. 2a). pericycle is discontinuous and the sieve tube In frontal view, the leaf cells are rectangular in the

Table 1 – Abiotic parameters of lotic and lentic environments where Potamogeton polygonus was sampled. Values refer to pH, water velocity (V), oxygen level (in % and mg/L), electricity (E), conductivity (C) and total salts dissolved (TSD).

Environment depth pH V O2 O2 E C TSD (m) cm/s (%) (mg/L) (mv) (ìS) (mg/L) Lentic 4 7.4 0 86.5 8.5 -16 31 16.7 Lotic 0.8 7.2 27 95.5 9.25 14 23.3 12.5

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Figures 1a-h – Root and stem of Potamogeton polygonus. a. Transverse section of the root, showing the epidermis (ep), exodermis (arrow), aerenchyma (ar), inner cortex (co) and vascular cylinder (vc). b. Detail of the epidermis (ep) with root hairs (rh) and exodermis with passage cells (*). c. Transverse section of the root with pentarch pattern, evidencing a central metaxylem element and a sieve tube element (st) in direct contact with the endodermis (*). d. Transverse section of the stem, showing the epidermis with chloroplasts, air lacunar and subepidermal fiber bundles (arrow). e. Diaphragm of stem aerenchyma, in frontal view. f. Detail of diaphragm cells, from Figure e. g. Diaphragm of stem aerenchyma, in longitudinal view. h. Transverse section of the stem, showing the organization of the six vascular bundles and protoxylem lacunae. Figures a, b, c, d and h are photomicrographs in light microscope, stained with toluidine blue. Figures e, f and g are electron micrographs in scanning electron microscopy. Scale bars = 50µm (except for Figure f, scale bar = 10µm).

Rodriguésia 62(4): 927-936. 2011 Morpho-anatomical adaptations of Potamogeton polygonus 931 Table 2 – Anatomical characteristics of Potamogeton polygonus root, stem and leaf in lotic and lentic environments. Data are given as mean ± standard deviation (n = 10). Letters stand for significant differences between specimens in the two environments (Student’s t test, P < 0.05). Characteristics Lotic environment Lentic environment Total plant heigth (cm) 37.29 ± 10.51 a 48.2 ± 11.54 b Internode length (cm) 1.45 ± 0.44 a 2.56 ± 0.87 b Leaf blade length (cm) 8.41 ± 1.82 a 9.39 ± 1.70b Leaf blade width (cm) 0.35 ± 0.06a 0.36 ± 0.06 a Leaf area (cm2) 2.23 ± 0.66 a 2.49 ± 0.89 b Stem diameter (cm) 0.39 ± 0.06 a 0.33 ± 0.04 b

Table 3 – Morphological characteristics of Potamogeton polygonus root, stem and leaf in lotic and lentic environments. Data are presented as mean ± standard deviation (n = 10). Letters stand for significant differences between specimens in the two environments (Student’s t test, p < 0.05).

Characteristics Lotic environment Lentic environment Exodermal wall thickness (µm) 0.92 ± 0.16 a 0.40 ± 0.16 b Lacunal area of the stem (%) 49.03 ± 0.05 a 44.92 ± 0.07 a Number of fiber bundles in the stem 32.5 ± 2.59 a 29.8 ± 3.06 a Wall thickness of the stem fibers (µm) 1.59 ± 0.26a 1.08 ± 0.22b Wall thickness of the leaf epidermis (µm) 1.37 ± 0.21a 0.83 ± 0.06b Thickness of the leaf central region (µm) 153.49 ± 17.9a 124.5 ± 15.1b Thickness of the leaf mesophyll (µm) 41.5 ± 3.3a 30.71 ± 4a Lacunal area of the leaf mesophyll (%) 35.29 ± 0.08 a 40.40 ± 0.07 b Number of fiber bundles in the leaf blade 44.4 ± 4.87 a 28.6 ± 0.89 b Wall thickness of the leaf fibers (µm) 1.48 ± 0.1a 0.93 ± 0.04b lentic environment (Fig. 2b), and quadrangular in Discussion the lotic environment (Fig. 2c). The mesophyll is Potamogeton polygonus exhibits several similar in both environments, formed by characteristics that differentiate individuals from aerenchyma in the central region (Fig. 2a) and by a lotic and lentic environments, both in terms of single layer of chlorophyllous parenchyma in the rest of the blade leaf (Fig. 2e-g). The leaf aerenchyma external morphology and anatomical structure. also exhibits diaphragms composed of arm-shaped Plants from the lotic environment are shorter and chlorophyllous cells, similar to those found in the have smaller leaf area, but larger stem diameter and stem. The aerenchyma in the leaves of the lentic leaf blade thickness. Similar morphological environment have a lacunal area proportionately adaptations were recorded in several species larger than the one in leaves of the lotic subjected to hydrodynamic stress (Idestam- environment (Table 3). In the leaf blade, fiber Almquist & Kautsky 1995; Schutten & Davy 2000; bundles and vascular bundles are alternated, and Gantes & Caro 2001; Puijalon & Bornette 2004; fiber bundles predominate (fig. 2d-e). On each Puijalon et al. 2005). Hydrodynamic forces can lead border, there is a large fiber bundle at subepidermal to convergence, due to plasticity or selection, which position (Fig. 2f-g). The vascular bundles are allows better performance in each environment. collateral and have a fiber cap in the periphery of Reduced size and greater stem thickness can the phloem and xylem (fig. 2a). The vascular bundle decrease risk of breakage and uprooting (Idestam- of the central region is more developed in the lotic Almquist & Kautsky 1995; Schutten & Davy 2000) environment, which results in greater leaf thickness and decrease resistance to water flow (Boeger & in this environment (Table 3). Poulson 2003). In P. polygonus, we also recorded a

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f g Figures 2a-g – Leaf of Potamogeton polygonus. a. Transverse section of the leaf blade, in the central region, showing epidermis (*), aerenchyma (ar) and vascular bundle (vb). b. Leaf blade surface (lentic environment), showing the rectangular shape of the epidermal cell. c. Leaf blade surface (lotic environment), showing the quadrangular shape of the epidermal cell. d. Transverse section of the leaf blade (lentic environment), showing fiber bundles in the mesophyll (arrow). e. Transverse section of the leaf blade (lotic environment), showing fiber bundles in the mesophyll (arrow). f. Transverse section of the leaf blade ( lentic environment), showing the fiber bundles in the leaf edge. g. Transverse section of the leaf blade ( lotic environment), showing the fiber bundles in the leaf edge. Figures a, d, e, f and g are photomicrographs in light microscopy, stained with toluidine blue. Figures b and c are electron micrographs in scanning electron microscopy. Scale bar = 50mm. higher number of fiber bundles in the leaves, that individuals of P. polygonus from lotic environments can be interpreted as an adaptive response that would not need to invest so much in apical growth increases resistance to hydrodynamic forces. and leaf area compared with those from lentic The aforementioned studies relate environments, as observed in the present study. In morphological adaptations only to water velocity, contrast, individuals from lentic environments are but the addition of information on light availability rooted in deeper substrates, and are potentially would be more elucidating. Puijalon & Bornette subjected to other factors that could reduce light (2004) suggested that plants that grow in availability, such as periphyton growth and environments with higher water velocity usually sedimentation of suspended particles on leaves. exhibit horizontal branches aligned with the stream. Studies show that there are similarities between the These authors explain that this inclination reduces responses of plants subjected to shade and resistance, but do not mention that it also increases submersion, since blade water depth acts as a the area exposed to solar radiation. Thus, light filter (Boeger & Poulson 2003; Mommer et

Rodriguésia 62(4): 927-936. 2011 Morpho-anatomical adaptations of Potamogeton polygonus 933 al. 2005). Spencer (1986) also showed that in P. (Sculthorpe 1967). They can be formed by a single cell pectinatus stem elongation rate is negatively layer (Bona & Alquini 1995 b; Evans 2003), by two or, related to solar radiation. occasionally, by three cell layers (Sculthorpe 1967). Aquatic plants also face hypoxia and exhibit Sculthorpe (1967) reported that in Potamogeton each different adaptive strategies to survive this stress. diaphragm is formed by one or occasionally two to Species with emergent or floating leaves, which have three cell layers. Diaphragms with one cell layer were fixed roots in anoxic sediments, depend on the internal also recorded in the leaves and stems of P. illinoensis transport of oxygen from leaves to roots through the Morong and P. gayi A. Benn. (Rodrigues 2006). system of air lacunae, whereas submersed species Diaphragms present in the aerenchyma, in addition to obtain these gases by diffusion (Rascio 2002). Leaves helping support it, seem to have other functions, such of submersed species can be entire, windowed or as the isolation of damaged internodes, preventing dissected (Sculthorpe 1967). Species that exhibit entire water from invading and damaging other parts of the leaves are frequently very thin and more or less plant (Sculthorpe 1967; Soukup et al. 2000). translucent, and do not have developed aerenchyma. Addition to hypoxia, another limiting factor In P. polygonus, the marginal regions of the leaf blade of submersed plants is the low solubility of carbon have only three layers of cells and the aerenchyma dioxide. However, to overcome this condition, many occurs only in the thicker central region. The lower submersed plants, including Potamogeton species, proportion of leaf lacunal area found in leaves from exhibit morphological and physiological the lotic environment in the present study can be adaptations to increase the input gas capacity related to higher oxygenation caused by turbulence (Sand-Jensen & Gordon 1984; Madsen & Sand- in this environment. Jensen 1991; Van den Berg et al. 2002; Rascio 2002). Several authors studied the origin and For P. polygonus, diaphragms can also be classification of the aerenchyma architecture in root important in the enlargement of areas for CO2 and stem of aquatic plants (Seago et al. 2005; Evans fixation, because they have chloroplasts, 2003; Jung et al. 2008). In the root of terrestrial corroborating what was previously suggested by flood-tolerant plants, the aerenchyma is frequently Scremin-Dias et al. (1999). Diaphragms with of lysigenous origin: some cells die and disappear, chlorophyllous cells were also recorded in leaves and forming air spaces (Evans 2003). However, in most stems of P. illinoensis and P. gayi (Rodrigues 2006). aquatic plants, the formation of the lacunae of the Many submersed species use the bicarbonate – lysigenous aerenchyma in the root occurs with the ion (HCO3 ) as an inorganic carbon source (Sand- collapse of cellular content, but with maintenance Jensen & Gordon 1984; Madsen & Sand-Jensen of the cell walls (Seago et al. 2005; Jung et al. 2008). 1991; Van den Berg et al. 2002; Rascio 2002). For – In the studied species, rows of radial cells collapse the input of HCO3 in the cell, a conversion of – maintaining their cell walls intact, and form an HCO3 into CO2 must occur in the cell wall or in the aerenchyma of the radial lysigenous type, according presence of a carrier protein in the plasmalemma. to the classification of Seago et al. (2005). It is For this reason, Rascio (2002) emphasizes that in – believed that in P. polygonus these walls have an species in which this route for the use of HCO3 important role in maintaining the shape and occurs, including species of Potamogeton, there is increasing the tensional force of the organ, likewise a thickening of the outer periclinal wall of the the diaphragms in stem and leaves. In this species, epidermal cells, with projections towards the the origin and architecture of the root aerenchyma interior of the cell, increasing the plasmalemma area. differ from that recorded of the stem and leaves. In The details of the projections of the walls of the stem, the aerenchyma is arranged as a epidermal-cells walls can only be observed in honeycomb. According to Seago et al. (2005), when transmission electron microscopy, but the this type of aerenchyma occurs in the roots, it thickening of the wall could be observed in the originated from the oblique division and expansion epidermal cells of the leaf and stem of P. polygonus. of the cells that surrounded the air lacunae, and is The stem vascular system of aquatic denominated expansigenous. However, Jung et al. angiosperms may seem to be reduced compared to (2008) state that in stems this type of aerenchyma does terrestrial species, even a fusion of vascular bundles not necessarily have homologous origin with the root. can occur in the center, resembling the stele of roots Diaphragms are widely found in stems and (Sculthorpe 1967). Schenck (1886 apud Sculthorpe leaves of aquatic plants, especially in 1967) states that this reduction in the stem vascular

Rodriguésia 62(4): 927-936. 2011 934 Lusa, M.G. et al. system represents an important mechanical demonstrated in previous studies with Ranunculus adaptation. In the genus Potamogeton several trichophyllus Chaix (Ranunculaceae) (Dalla stages of fusion and reduction of vascular bundles Vecchia et al. 1999) and other species of are observed, characteristics that are important for Potamogeton (Chambers et al. 1989; Idestam- the systematics of the group (Sculthorpe 1967; Almquist & Kautsky 1995). Wiegleb 1990; Kaplan 2001). Wiegleb (1990) The presence of Caspary strips in endodermal describes four types of stele: the proto type, with cells of stem and leaf of P. polygonus is common four (rarely three) median bundles and three (5-6) also in other aquatic plants (Sculthorpe 1967). In lateral bundles, as recorded in Potamogeton aquatic plants, this layer may have the function of pulcher Tuckerman; the type with 8 bundles, in ionic selectivity, but can also be a barrier to the exit which three median bundles fuse, e.g. P. natans of gases from the vascular cylinder and to the Thunb.; the oblong type, in which the stele is not entrance of pathogens (Esnault et al. 1994; Dalla- lobed and the bundles are grouped into three Vecchia et al. 1999; Enstone et al. 2003). Frank & groups, e.g. L.; and the type Hodgson (1964) investigated the absorption of with four bundles, recorded by the author only in herbicides marked with 14C, in different parts of Australian species of the complex P. cheesemanii specimens of P. pectinatus, and confirmed the A. Bennett. The species P. pectinatus was not cited absorption capacity of leaves in addition to roots. in the study of Wiegleb (1990), but Sculthorpe A neglected characteristic, both for (1967) emphasizes that in this species a more or aerenchymatous and non-aerenchymatous roots of less homogeneous phloem zone occurs, aquatic plants, is the mechanical function of wall surrounding a central axial lacuna. Kaplan (2001) thickening in cortex cells, in addition to the used characteristics of the stem’s stele to endodermis and exodermis. In the case of Caltha distinguish the hybrid P. x fluitans Roth from its palustris L.(Ranunculaceae), the cortex has no parietals P. natans and P. lucens. The pattern found aerenchyma and the cells of the inner cortex have in P. polygonus is consistent with the description slight wall thickening (Seago et al. 2000). In of the oblong type by Wiegleb (1990). Nymphaea odorata Aiton (Nympheaceae), lignified In many Potamogeton species cortical sclereids, close to the endodermis, provide the interlacunar and subepidermal vascular bundles mechanical support (Seago et al. 2000). In the roots occur (Sculthorpe 1967; Kaplan 2001; Alix & Scribailo of P. polygonus the mechanical layers, which exhibit 2006). These bundles do not occur in P.crispus L. wall thickening, are the endodermis and exodermis. (Alix & Scribailo 2006) nor in P. polygonus. The greater wall thickening in P. polygonus in lotic In roots of aquatic monocotyledons the environments is consistent with its association with polyarch stele also exhibits a reduction in the number mechanical resistance. of arches and even a complete absence of medullar parenchyma. Sauvageau (1894 apud Sculthorpe 1967) Ackowledgements studied the progressive reduction of this system in CNPq (Brazilian Research Council) funded this roots of Potamogeton and found that in P. natans study (Edital Universal CNPq no 019/2004) and granted and P. pectinatus the stele is pentarch, as also productivity fellowships to Dr. Cleusa Bona and Dr. recorded for P. polygonus in the present study. Maria Regina Boeger; Instituto Ecoplan and Fundação The reduction of the root vascular system Pizzatto provided logistic support during fieldwork. does not indicate, necessarily, a reduction in the capacity of absorption of water and solutes. The References presence of root hairs located in front of exodermal passage cells, recorded in P. polygonus, indicates Alix, M.S. & Scribailo, R.W. 2006. First report of Potamogeton x undulatus (P. crispus x P. that there is a potential regulation of the lateral flow praelongus, Potamogetonaceae) in North America, of water and ions in roots. It has been shown that with notes on morphology and stem anatomy. in most aquatic species the exodermis has similar Rhodora 108: 329-346. functions similar to the endodermis (Esnault et al. Berlyn, G.P. & Miksche, J.P. 1976. Botanical 1994; Kamula et al. 1995; Seago et al. 2000; Enstone microtechnique and cytochemistry. The Iowa State et al. 2003; Soukup et al. 2007). The importance of Press, Ames. 326p. the sediment as a source of essential minerals for Boeger, M.R.T. & Poulson M. E. 2003. Morphological rooted submersed aquatic plants has already been adaptations and photosynthetic rates of amphibious

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Artigo recebido em 27/04/2011. Aceito para publicação em 01/09/2011.

Rodriguésia 62(4): 927-936. 2011